Download Distribution patterns of five zoanthid species in Okinawa Island, Japan

Zoological Studies 50(4): 426-433 (2011)
Distribution Patterns of Five Zoanthid Species at Okinawa Island, Japan
Yuka Irei1,*, Yoko Nozawa2, and James D. Reimer3
Molecular Invertebrate Systematics and Ecology Laboratory, Graduate School of Marine Science, Univ. of the Ryukyus, Senbaru 1,
Nishihara, Okinawa 903-0213, Japan
2
Biodiversity Research Center, Academia Sinica, Nankang, Taipei 115, Taiwan
3
Molecular Invertebrate Systematics and Ecology Laboratory, Rising Star Program, Transdisciplinary Research Organization for
Subtropical Island Studies (TRO-SIS), Univ. of the Ryukyus, Senbaru 1, Nishihara, Okinawa 903-0213, Japan
1
(Accepted March 9, 2011)
Yuka Irei, Yoko Nozawa, and James D. Reimer (2011) Distribution patterns of five zoanthid species at
Okinawa Island, Japan. Zoological Studies 50(4): 426-433. Zoanthids (Anthozoa, Hexacorallia) are distributed
worldwide, especially in shallow tropical and subtropical waters. In fringing reefs of Okinawa I., southwestern
Japan, zoanthids are common benthic organisms. Despite their abundance, even basic ecological information
such as favorable habitats based on quantitative surveys is still lacking. Accordingly, we investigated the
distribution patterns of 5 common zooxanthellate zoanthid species in shallow reef waters (< 10 m) of Okinawa
I.: Palythoa tuberculosa, P. mutuki, Zoanthus sansibaricus, Z. kuroshio, and Z. gigantus. The survey was
conducted using the belt transect method in 3 reef environments (moat, reef crest, and reef slope) at 10 reef
sites in 2008. As a result, 2404 zoanthid colonies were observed, and Z. sansibaricus and P. tuberculosa were
the 2 most dominant species, respectively comprising 52% and 41% of the total zoanthids observed. The
environment where the highest numbers of colonies were observed was the reef crest (1615 colonies) followed
by the reef slope (687 colonies), while zoanthids were rare in the moat environment (102 colonies). There were
significantly more Z. sansibaricus colonies on reef crests than reef slopes, but no significant difference was
seen in the frequencies of the other 4 species between the reef crest and reef slope. As to the zoanthid colony
size, most colonies (> 86%) of the 5 zoanthid species were < 10 cm in diameter, and only 2 colonies of > 50 cm
in diameter were observed in the survey. The absence of zoanthids in moats suggested that sedimentation
or weak currents may be factors limiting zoanthid distribution; however, detailed investigations are necessary
to confirm this. Since zooxanthellate zoanthids are a major benthic group on coral reefs, further research
focusing on the relationships between zoanthid distribution and environmental conditions will foster a better
understanding of coral reef ecosystems. http://zoolstud.sinica.edu.tw/Journals/50.4/426.pdf
Key words: Zoanthid, Distribution, Shallow reef environment, Belt transect.
Z
oanthids (Anthozoa, Hexacorallia) are
an order of cnidarians characterized by having
2 rows of tentacles and 1 siphonoglyph, and are
generally colonial with polyps linked by common
tissue (a coenenchyme). Additionally, most
zoanthids incorporate grains of sand from their
environment into their body structure. Due to
these unique characters, zoanthids are often
referred to as encrusting anemones. Zoanthids
are distributed in most marine environments, from
temperate to tropical areas and from the intertidal
zone to the deep sea below 5000 m, and are
particularly common in tropical and subtropical
seas (Fosså and Nilsen 1998, Reimer and Miyake
2009). In total, 354 zoanthid species were
reported worldwide (Fautin 2010); however, the
number of proper species is likely much less due
to inadvertent re-descriptions (Burnett et al. 1997,
Reimer et al. 2004). In shallow waters surrounding
Okinawa I., southwestern Japan, there are at least
*To whom correspondence and reprint requests should be addressed. Tel: 81-98-8958542. Fax: 81-98-8958577.
E-mail:[email protected]
426
Irei et al. – Distribution of Zoanthids at Okinawa
13 species (including undescribed species) of
brachycnemic zoanthids from 5 genera: Palythoa,
Zoanthus, Sphenopus, Isaurus, and Neozoanthus
(Reimer 2010).
The genera Palythoa and Zoanthus are
common benthic taxa in coral reefs and have
large influences on other benthos by covering
them or limiting space availability (Suchanek and
Green 1981). Several studies related to zoanthid
population dynamics, dispersal strategies, and
possible influences on coral reef ecosystems
were conducted in the Atlantic (Acosta 2005,
Mendonça-Neto et al. 2008) and Caribbean
(Sebens 1982, Karlson 1983, Bastidas and Bone
1996). In the Indo-Pacific; however, quantitative
surveys focusing on zoanthid distributions are
almost nonexistent despite the general abundance
of zoanthids. Ono et al. (2003) performed longterm monitoring of the coverage of Zoanthus
sansibaricus in Kagoshima, Japan. However,
their monitoring area was quite limited as only
1 transect (1 × 50 m) was examined. As to
distribution patterns of zoanthids in Japan, P.
tuberculosa being able to inhabit a wide depth
range from the intertidal zone to over 30 m in depth
at Okinawa was only briefly mentioned (Reimer et
al. 2007b), and Z. sansibaricus has mainly been
reported on reef crests (Reimer 2008). To verify
such observations and gain additional information,
this study examined distribution patterns of 5
common zooxanthellate zoanthid species on 3
typical coral reef environments (moat, reef crest,
and reef slope) at 10 locations around Okinawa I.,
southwestern Japan.
MATERIALS AND METHODS
Five zooxanthellate zoanthids, Palythoa
tuberculosa Klunzinger 1877, P. mutuki Haddon
and Shackleton 1891, Zoanthus sansibaricus
Carlgren 1900, Z. kuroshio Reimer and Ono 2006,
and Z. gigantus Reimer and Tsukahara 2006
(Fig. 1), were examined in this study. Species
identifications were sensu Reimer et al. (2006a
2007b). All 5 species possess endosymbiotic
Symbiodinium spp. dinoflagellates (Reimer et al.
2006b 2007a b) and form colonies attached to
hard substrates such as rocks or compacted coral
of coral reefs.
This study was conducted at 10 coral reef
sites around Okinawa I., southern Japan (Fig.
2A). The environment of shallow coral reef sites
427
on Okinawa I. generally differ between the east
and west coasts. In contrast to well-developed
coral reefs on the west coast, ocean floors of
many sites on the east coast are muddy and/or
sandy, and zooxanthellate zoanthids are generally
uncommon. Therefore, the 10 study sites were
chosen mainly from the west coast of Okinawa
I. (Fig. 2A). Surveys were performed between
14 Apr. and 4 Dec. 2008. Okinawan coral reefs
are largely fringing reefs with developed moats,
and thus in this study, we conducted surveys in
3 different reef environments at each site: moat,
reef crest (the elevated area located outside of the
moat), and reef slope (the area located outside
the reef edge) (Fig. 2B). The depth range of each
reef environment we surveyed was 1-3 m in the
moat, 0-2 m on the reef crest, and 5-10 m on the
reef slope. In this study, we utilized 10 × 1-m belt
transects and counted the number of colonies of
the 5 zooxanthellate zoanthid species. First, a
10-m line was randomly set parallel to the reef
edge. Then a 0.5-m width was defined on each
side of the line by the length of the observer’s
outstretched arms. Nine transects were set at
each study site, with 3 transects for each reef
environment (moat, reef crest, and reef slope). In
three (Maeda-west, Mizugama, and Sunabe) of the
10 studied reef sites where the moat was not well
developed, only the reef crest and reef slope were
surveyed. In general, percentage coverage is
often calculated in quantitative surveys of sessile
benthic organisms using photography or video.
However, in this study, colony numbers were
utilized instead because analyzing photographic
images was very difficult due to the generally
small sizes of the colonies and choppy conditions
on the reef crests. Observations and counts of
colonies were performed in situ by scuba diving or
snorkeling. The data obtained were recorded on
waterproof paper.
To determine the size frequency distributions
of the species, the general colony size was also
recorded using 5 size categories at eight of 10
study locations, with the exception of Zanpa and
Minatogawa. The 5 categories (SS, S, M, L, and
LL) were defined as follows: SS, fewer than 10
polyps; S, more than 10 polyps of 10 × 10 cm; M,
10 × 10-25 × 25 cm; L, 25 × 25-50 × 50 cm; and
LL, > 50 × 50 cm. Each colony size was estimated
with a ruler and assigned to a size class.
From previous studies, asexual reproduction
by fragmentation is known for some Zoanthus
and Palythoa species (Karlson 1986, Acosta et
al. 2001). Their fission processes and triggers
Zoological Studies 50(4): 426-433 (2011)
428
inducing fragmentation were previously studied,
especially for mat-like Palythoa species such
as P. caesia on the Great Barrier Reef (Tanner
1997) and P. caribaeorum in the Atlantic (Acosta
2005). Those 2 species have very similar
morphologies to P. tuberculosa, in possessing
a thick and well-developed coenenchyme. In
shallow reefs of Okinawa I., large aggregations of
small P. tuberculosa colonies exist, implying that
fragmentation may often occur. Numerous small
polyp-clusters forming large aggregations may be
genetically identical. However, it is impossible to
distinguish clone colonies in the field. Thus, the
definition of an “identical colony” was defined as “all
polyps connected by a continuous coenenchyme”
in this study. However, in some cases, the juncture
of the polyps could not be observed due to the
complexity of the substrate and small stoloniferous
connections of the polyps. In such a situation,
zoanthid polyps within a 5-cm radius were defined
as being identical. However, adjoining zoanthid
polyps were defined as belonging to different
colonies when their oral disk colors obviously
differed from each other. Considering the colony
size, morphological characters of the 5 zoanthid
species in this study were noted. Unlike the mat-
(A)
(B)
(C)
(D)
(E)
Fig. 1. Five zoanthid species investigated in this study. (A) Palythoa tuberculosa (at Sunabe), (B) P. mutuki (at Odo), (C) Zoanthus
sansibaricus (at Oyama), (D) Z. kuroshio (at Maeda-east), (E) Z. gigantus (at Oyama). Scale bar = 1 cm.
Irei et al. – Distribution of Zoanthids at Okinawa
429
JAPAN
(A)
Eastern China Sea
Okinawa l.
128°00'E
TAIWAN
a
26°30'N
b
e dc
f
g
h
PHILIPPINESS
N
250 km
j
i
10 km
(B)
M
Shore
RC
RS
Offshore
Fig. 2. Study locations investigated in this study. (A) Locations investigated at Okinawa I.: (a) Oku (26°50'58.53"N, 128°16'54.48"E),
(b) Manza (26°30'06.93"N, 127°50'32.86"E), (c) Maeda-east (26˚26'42.29"N, 127°46'07.75"E), (d) Maeda-west (26°26'36.40"N,
127°46'22.80"E), (e) Zanpa (26°26'29.56"N, 127°42'44.04"E), (f) Sunabe (26°19'46.97"N, 127°44'35.14"E), (g) Mizugama
(26°21'34.28"N, 127°44'20.13"E), (h) Oyama (26°17'08.07"N, 127°44'22.40"E), (i) Minatogawa (26°07'11.65"N, 127°45'41.97"E), (j)
Odo (26°05'13.11"N, 127°42'36.72"E). (B) Typical geographical structure of a fringing reef and the 3 topographic zones investigated in
this study: M, moat; RC, reef crest; RS, reef slope.
Zoological Studies 50(4): 426-433 (2011)
430
moat environment (Table 1). Distribution patterns
of the 5 zooxanthellate zoanthid species in the
2 reef environments were analyzed using the
Wilcoxon matched-pairs test. Because the same
analysis was employed for all 5 zoanthid species,
the significance level was adjusted by dividing the
original significance level by 5 according to the
Bonferroni method. Size-frequency distributions
were compared between the 2 dominant species,
P. tuberculosa and Z. sansibaricus, using the
Kolmogorov-Smirnov test. Size-frequency
distributions of P. tuberculosa found on the reef
crest and reef slope were also compared using the
Kolmogorov-Smirnov test, as sufficient numbers
of colonies were present in both environments. All
size data recorded for each of the categories in
this study were pooled and used for comparisons.
STATISTICA (vers. 9.0) software (StatSoft, Tulsa,
OK, USA) was used for the statistical analyses.
like P. tuberculosa with tightly joined polyps, the
other 4 species in this study and particularly
P. mutuki had thinner coenenchymes and less
densely packed polyps, and this may have
enhanced colony diameter sizes. However, this
likely did not affect the results of this study since
colony size categories were relatively roughly
estimated with wide-ranging size classes.
Although data (number of colonies) were
collected using 3 replicate transects in each of
the 3 reef environments, resultant data from the
3 replicate transects were pooled and used in
subsequent analyses due to the large variation
among the replicates and the occurrence of many
0 values (i.e., no colony observed on the transect)
in the data. When analyzing distribution patterns
among the 3 reef environments, comparisons
were only made between the reef crest and reef
slope, because few colonies were observed in the
Table 1. Colony numbers of 5 zoanthid species belonging to the genera Palythoa and Zoanthus, observed
in a 30-m2 area of 3 coral reef zones (M, moat; RC, reef crest; RS, reef slope) at 10 sites around Okinawa
I. Sites are listed in order of latitude from north to south. *The moat was not surveyed due to the lack of the
zone at these sites
P. tuberculosa (n = 988)
Palythoa
P. mutuki (n = 86)
Sites
M
RC
RS
Total
M
RC
RS
Total
Oku
Manza
Maeda-east
Maeda-west*
Zanpa
Mizugama*
Sunabe*
Oyama
Minatogawa
Odo
Total
1
2
0
0
0
0
1
4
124
1
3
58
15
91
37
2
8
17
356
61
27
5
69
27
63
5
0
216
155
628
186
30
8
127
42
154
42
2
224
173
988
65
0
0
0
0
0
0
65
17
0
0
1
1
0
1
0
1
0
21
0
0
0
0
0
0
0
0
0
0
0
82
0
0
1
1
0
1
0
1
0
86
Zoanthus
Z. sansibaricus (n = 1253)
Z. kuroshio (n = 54)
Z. gigantus (n = 23)
Sites
M
RC
RS
Total
M
RC
RS
Total
M
RC
RS
Total
Oku
Manza
Maeda-east
Maeda-west*
Zanpa
Mizugama*
Sunabe*
Oyama
Minatogawa
Odo
Total
5
27
1
0
0
0
0
33
38
58
176
230
41
94
21
70
224
255
1207
1
1
0
11
0
0
0
0
0
0
13
44
86
177
241
41
94
21
70
224
255
1253
0
0
0
0
0
0
0
0
0
0
0
2
8
0
0
1
0
2
13
1
9
5
15
5
0
0
2
4
0
41
1
9
5
17
13
0
0
3
4
2
54
0
0
0
0
0
0
0
0
8
0
1
0
2
3
0
4
0
0
18
2
1
0
1
0
0
0
0
1
0
5
10
1
1
1
2
3
0
4
1
0
23
Irei et al. – Distribution of Zoanthids at Okinawa
RESULTS
1). In the moat environment, the density of each
zoanthid species was 0-5 colonies/30 m2, except
for P. mutuki at Oku (65 colonies/30 m2) and Z.
sansibaricus at Manza (27 colonies/30 m2). Of the
5 zooxanthellate zoanthid species examined, only
Z. sansibaricus showed a significant difference in
the number of colonies between the reef crest and
reef slope environments. There were significantly
more colonies of Z. sansibaricus on the reef crest
than reef slope (pre-adjusted p < 0.01, adjusted by
the Bonferroni method p < 0.05, n = 10 sites) (Table
1). Although the same trend was also seen with P.
mutuki (i.e., more colonies on the reef crest), the
result was not statistically significant after adjusting
the significance level by the Bonferroni method (cf.
pre-adjusted p < 0.05, n = 5 sites).
Small (S)-sized colonies were the most
frequent for all 5 zooxanthellate zoanthid species
(Fig. 3). For P. mutuki and Z. gigantus, frequencies
of SS colonies were also high (Fig. 3). In terms
of the 2 dominant species (P. tuberculosa and Z.
In total, 2404 zoanthid colonies were
observed from the 81 transects (with a total
surveyed area of 810 m2) recorded in this study.
Zoanthus sansibaricus was the most dominant
species (1253 colonies), making up 52% of
the total colony number, followed by Palythoa
tuberculosa (988 colonies; 41%) (Table 1). The
3 remaining species combined to make up < 7%
of the total colony number. There were large
variations and no obvious trend in colony numbers
of each zoanthid species among the 10 study sites
(Table 1). Large variations were also seen in the
number of zoanthid colonies among the 3 replicate
transects in each reef environment, resulting in
many 0 values recorded in the replicate transects
(data not shown). Among the 3 reef environments
at Okinawa I. examined in this study (moat, reef
crest, and reef slope), most zoanthid colonies were
observed on the reef crest and reef slope (Table
P. tuberculosa
600
431
P. mutuki
50
40
400
30
20
200
Colony number
10
0
SS
S
M
L
LL
Z. sansibaricus
800
0
SS
S
M
L
LL
Z. kuroshio
40
600
30
6
400
20
4
200
10
2
0
SS
S
M
L
LL
0
SS
S
M
Z. gigantus
8
L
LL
0
SS
S
M
L
LL
Size categories
Fig. 3. Size-frequency distributions of 5 zooxanthellate zoanthid species observed in this study. Size categories: SS, fewer than 10
polyps; S, more than 10 polyps at 10 × 10 cm; M, 10 × 10-25 × 25 cm; L, 25 × 25-50 × 50 cm; LL, > 50 × 50 cm.
Zoological Studies 50(4): 426-433 (2011)
432
sansibaricus), we found no significant difference in
size class ratios between the 2 species (p > 0.1)
(Figs. 3A, C). In addition, colony sizes of P.
tuberculosa found on the reef crest and reef
slope were compared, since sufficient numbers
of colonies were present in both environments.
Again, no significant differences were seen
between the 2 reef environments (p > 0.1) (Fig. 4).
DISCUSSION
In this study, distribution patterns of 5
zoanthid species were surveyed among 3 different
reef environments (moat, reef crest, and reef
slope) at 10 sites around Okinawa I. Colony
numbers of each zoanthid species greatly varied
from site to site, suggesting a patchy nature of
distribution for the 5 zoanthid species. Despite
this, distribution patterns among the 3 reef
environments were generally consistent and
clear for all 5 species among different sites.
Palythoa tuberculosa and Z. sansibaricus were
numerous on coral reefs of Okinawa. From the
frequency in each environment, the main habitat
of Z. sansibaricus was the reef crest, while P.
tuberculosa was observed on both reef crests and
reef slopes. Thus, in general, it appears that P.
tuberculosa has a vertically wider distribution than
Z. sansibaricus around Okinawa I. These results
are similar to the theory proposed by Reimer et
al. (2006b), in which P. tuberculosa was surmised
to be a “generalist” based on observations of P.
tuberculosa in various environments in southern
Japan as well as on the presence of subclades
400
RC
RS
Colony number
300
200
100
0
SS
S
M
L
LL
Fig. 4. Size-frequency distributions of colonies of Palythoa
tuberculosa observed in 2 reef environments (RC, reef crest;
RS, reef slope). Size categories: SS, fewer than 10 polyps; S,
more than 10 polyps at 10 × 10 cm; M, 10 × 10-25 × 25 cm; L,
25 × 25-50 × 50 cm; LL, > 50 × 50 cm.
C1 and C3 Symbiodinium within P. tuberculosa
colonies, which are relatively common among
various zooxanthellate anthozoans in the IndoPacific and Atlantic-Caribbean (LaJeunesse
2005). It was difficult to conclusively determine the
habitats of the 3 remaining species; P. mutuki, Z.
kuroshio, and Z. gigantus, between the reef crest
and reef slope (but clearly not the moat), due to
their low total numbers observed in this study.
There are likely various environmental factors
that determine the distribution patterns of zoanthid
species. It was shown that water temperature
(Ono et al. 2003), sedimentation (Sebens 1982,
Ono et al. 2003), predation (Sebens 1982), and
desiccation stress during low tides (Sebens 1982)
affect zoanthid distributions. In moats, only a
few colonies were recorded, and sedimentation
or unfavorable salinity could have been cause of
this. For example, due to generally weak currents
in moats, the substratum was often covered by
drifted sand (Takahashi 1988, Nakai 2007), making
survival of zoanthids and other benthic cnidarians
difficult. Moreover, moats are often affected by
runoff of fresh water from terrestrial ecosystems,
which lowers the salinity and in Okinawa, causes
red clay/sand sedimentation particularly after
heavy rains. As the water circulation in moats is
relatively poor (Nakai 2007), such unfavorable lowsalinity conditions can persist for a relatively longer
period than on the reef crest or reef slope. Thus,
such harsh conditions may limit the number of
colonies of zoanthids in moats. At Oku and Manza;
however, relatively large numbers of zoanthid
colonies were observed in the moats. The moats
at these 2 sites have relatively higher water flow,
and thus they may be similar environments to reef
crests (e.g., more favorable for zoanthids).
In this study, the frequency of zoanthid
species was determined from colony numbers on
the transects. Although we did not investigate
coverage, the frequency may be able to be
assumed to roughly correspond to the relative
cover of each zoanthid species, as most of
the colonies were in the SS and S categories.
Studies similar to the research performed here
with more-quantitative investigations of zoanthids
are needed in other regions of the world to better
understand the fundamental ecology of these
important coral reef organisms. Moreover, these
zooxanthellate zoanthids can be utilized as
environmental indicators for coral reef health since
they are common and abundant in coral reefs.
Additional research in future studies, such as
detailed environmental investigations and rearing
Irei et al. – Distribution of Zoanthids at Okinawa
experiments of zoanthids, will help elucidate
which environmental factors control the observed
distributional patterns of zoanthids.
Acknowledgements: The authors would like to
extend their gratitude to Dr. F. Sinniger and Mr.
Y. Tanaka who helped with fieldwork and gave
invaluable advice during this study. We also thank
E. Shiroma and all MISE Laboratory members
who helped with field work. The senior author was
funded by a grant-in-aid from the Japan Society for
the Promotion of Science (Wakate B #21770089)
and the Rising Star Program at the Univ. of the
Ryukyus.
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